[no]
THE ROLE OF THE COELOMIC FLUID IN THE
MOVEMENTS OF EARTHWORMS
BY G. E. NEWELL
From the Zoology Department, Queen Mary College, University of London
{Received 4 August 1949)
(With One Text-figure)
INTRODUCTION
The manner in which earthworms move on the surface of the soil is now well known,
for a brief but substantially correct account was given as long ago as 1894 by
Friedlander and again in 1901 by Bohn. Further details and an account of the
method by which co-ordination of the muscular movements is brought about have
been given by Gray & Lissmann (1938a). Darwin's (1881) account still remains the
best source of information on the burrowing of earthworms, but he was chiefly
concerned with their habits and only to a lesser degree with the mechanics of
burrowing. He gives, however, some valuable data on the times taken by worms to
burrow into different kinds of soil and confirms an observation of Perrier that the
anterior end of the body of the worm ia first attenuated and thrust a little way into
the soil and then expanded so that the soil is pushed away on all sides. Darwin also
brought forward strong evidence for the view that burrowing into very compact
soils is effected by the worms literally eating their way through it.
In a previous paper (Chapman & Newell, 1947) an attempt was made to describe
the functioning of the body fluid-muscular system of the lugworm, and it was shown
that even in inactive worms the body-wall muscles had a tonus sufficient to maintain
a distinct positive pressure in the coelomic fluids. During movement, particularly
during burrowing, the internal pressures rose to much higher figures, and from these
calculations could be made of the thrusts which could be exerted against the substratum. It was believed, therefore, that measurements of the internal pressures
developed in earthworms during movement and a knowledge of the way in which
pressure changes are distributed about the body would help in an understanding of
the mechanics of movement not only of these but of other animals with a similar
body plan.
An essential preliminary to an understanding of the role of the coelomic fluid in
the locomotion of the earthworm is a knowledge of the morphological relations of
the coelomic compartments and of the structure of the septa, particularly of their
musculature and of any perforations which may exist in them. In the lugworm,
where septa are absent from the greater part of the body, circulation of the coelomic
fluid is in no way impeded, and during burrowing fluid is driven forwards into the
more active anterior segments, thus increasing the possibility of greater forward
The role of the coelomicfluidin the movements of earthworms
111
extension and thrust when the circular muscles of the body wall contract against it.
At first sight such a redistribution of the coelomic fluid would appear to be impossible in a septate animal like the earthworm, but the possibility of communication
between the serially repeated coelomic compartments cannot be ruled out. Unfortunately, incomplete accounts only have been given of the septa of the lumbricidae
although the septa of some oligochaetes (e.g. those oiPheretima) have been described
in considerable detail. It was found necessary, therefore, to re-examine the septa in
earthworms.
THE COELOM AND SEPTA IN EARTHWORMS
A few anatomical features of Lumbricus terrestris may not be out of place. As is well known
the coelom of Lumbricus is a fairly spacious fluid-filled cavity extending throughout
practically the whole length of the body. In front of segment 5, however, its volume is so
reduced by a complicated musculature stretching from the pharynx to the body wall that
it is virtually occluded. The coelom communicates with the exterior by three sets of
apertures; the nephridiopores, the dorsal pores and the gonoducts. The nephridiopores, of
which there is one pair in every segment except the first three and last one, are minute
8phinctered apertures lying just anterior to the ventral chaetae; the dorsal pores, absent
from the first ten segments, lie in the mid-dorsal line and open through the anterior part of
each segment (not in the intersegmental position as is often stated). The oviducts have
a direct opening from the general perivisceral cavity in segment 13, but the vasa deferentia
lead to the exterior from the testis sacs which are coelomic compartments completely
closed from the general body cavity.
Behind segment 5, and throughout the rest of the body, the coelom is divided into
segmental chambers by septa running from the body wall to become inserted into the wall
of the gut. Each septum consists essentially of an anterior and a posterior layer of peritoneum, between which are muscles and connective tissue. The septa also carry blood
vessels, notably the dorso-subneural commissures, as well as segmental nerves. Ventrally
each septum is perforated by an aperture through which passes the ventral nerve cord.
De Ribaucourt (1901) has given a relatively complete account of the gross structure of
the septa in Lumbricus and other forms. He includes details of the histology and states that
in the genus Lumbricus the septa are not so strongly developed as in Allolobophora and
certain related genera. He believed that the septal muscles take origin from the longitudinal
muscles of the body wall of which they seem to be extensions. Septal muscles are more
pronounced near to the body wall and less so where the septa join the gut. Circular
muscles are only feebly developed and lie chiefly towards the posterior face of each septum
and are lacking altogether from its ventral part. Other septal muscles are not clearly
described by de Ribaucourt, and the only figures given are of sections of the septa, so that
his account does not form a good basis for the assigning of functions to the septal muscles.
It seemed necessary, therefore, to re-examine the septa in the earthworm.
THE STRUCTURE OF THE SEPTA
The structure of the septa was examined by dissection under a binocular microscope of
worms fully narcotized with 8 % magnesium sulphate and killed by slow injection of 5 %
formaldehyde. This treatment left the worms extended and the septa well stretched.
The existence of a ventral perforation in each septum around the nerve cord was verified.
This perforation is here termed the ventral foramen. Its upper boundary is clearly
indicated by the paired ventroparietal vessels which run in it. Also, in the region of the
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G.
E.
NEWELL
testis sacs, where the ventral vessel parts company with the ventral nerve cord, to run
dorsally to the testis sacs, an additional, but smaller, foramen exists in septa 9/10,10/11 and
11/12 to allow of a space around the vessel.
The septa as far back as the ioth segment are stouter and more muscular than those from
the ioth to the 19th segment, whilst septa 19/20, 20/21 and 21/22, which are attached to
the posterior part of the gizzard, are particularly muscular, being the stoutest septa in the
body. In addition to their intrinsic musculature the septa between all segments anterior to
segment 8 are provided with slips of muscle which leave the posterior face on each side of
Rod. mute.
J.W.
Obi. muse.
Sph. muse.
V.N.C.
V. for.
Ore. muse.
Fig. 1. Diagram to show the arrangement of the septal muscles: B.W., body wall; Ore. mute, circular
muscles; 06/. mute., oblique muscles; Rod. mute., radial muscles; Sph. muse., sphincter of ventral
foramen; V.for., ventral foramen; V.N.C, ventral nerve cord.
the body and traverse the coelom before becoming attached to the lateral body wall. Septa
anterior to that dividing segment 13 from 14 have, in addition, a short strand of muscle
attached to each side of the ventral foramen and running posteriorly to become attached to
the ventral body wall about half-way along the segment. In the region of the pharynx
numerous strands of muscle, probably concerned with the retraction of the pharynx, run
from it through the first three septa to join the muscles of the body wall. Despite these
variations, the general structure of the septa is nearly constant and for the purposes of the
present discussion it is sufficient to describe a typical septum.
The intrinsic musculature of the septa was examined partly in septa dissected out from
The role of the coelomc fluid in the movements of earthworms
113
the body and mounted as flat as possible on a slide, and partly from thick and thin microtome sections of complete worms. By these means it was verified that no perforation in the
septum exists, apart from the ventral foramen and those allowing the passage of the ventral
vessel in the region of the testis sacs.
The various sets of muscles which are arranged between the anterior and posterior
layers of peritoneum are conveniently described as if they were viewed either from the
front or rear of the septum, that is, as they would be seen in surface view of a stretched and
flattened preparation. Four sets of muscles were recognized (Fig. i).
(1) Radial muscles. Throughout the major part of each septum, strands of muscle run in
a radial direction from the body wall to the gut. They are much more numerous in the
dorsal part than elsewhere in the septum, gradually decreasing in number towards its
ventral part and absent altogether from the neighbourhood of the ventral foramen. In the
ventral parts of the septum the radial fibres depart from their truly radial orientation and
curve ventrally towards the body wall so that they form a series of arcs from the ventral
border of the gut to the ventro-lateral body wall.
(2) Circular muscles. Concentrically arranged series of circularly running fibres are
found throughout the septum, but they are interrupted ventrally by the ventral foramen.
(3) Sphincter muscle of the ventral foramen. Surrounding the ventral foramen, except on
its mid-ventral boundary, is a prominent band of muscle fibres which appears to be
a specialized part of the system of radial muscles of the septum, since at the borders of this
sphincter the fibres pass by almost imperceptible changes of direction into the series of
radial fibres.
(4) Oblique muscles. On each side of the mid-line bundles of muscle fibres fan out from
their attachments to the ventral body wall and pass obliquely dorsalwards to become
attached to the dorso-lateral body wall.
Despite a statement by de Ribaucourt (1901) that the septal muscles take origin from the
deeper layers of the longitudinal muscles of the body wall, the evidence derived from an
examination of sections seemed to show that it is to the bed of circular body-wall muscles
that they are connected.
FUNCTIONS OF THE SEPTAL MUSCLES
It will be apparent from the description of the septal musculature that the circular
radial and oblique fibres would provide a means whereby the septum could remain
taut whilst the diameter of the body is being varied by the reciprocal action of the
circular and longitudinal muscles of the body wall. The radial muscle fibres,
inserted as they are in the peritoneum of the gut, may also play a part in restricting
the occlusion of the gut lumen by the positive pressure of the coelomic fluid. It also
is evident that the oblique muscles of the septum, when in a state of contraction, will
tend to produce a dorso-ventral flattening of the body.
Unfortunately, attempts to obtain direct experimental evidence of the action of
the septal muscles by electrical stimulation failed, since the stimulus used always
evoked a simultaneous contraction of the longitudinal muscles of the body wall.
This causes the body to become shorter but fatter, stretches the septa and masks
any contraction of their intrinsic musculature, if, indeed, it takes place at all.
The evidence regarding the action of the septal muscles during locomotion is,
therefore, indirect.
It seems reasonable to assume that the septa in an earthworm would behave,
JBB. 37, I
8
ii4
G. E. NEWELL
during locomotion, in a manner essentially similar to those of small aquatic oligochaetes such as Tubifex. In this worm direct observation of the septa is rendered
possible by the transparency of the body wall, and it can be seen that during locomotion the septa undergo considerable distortion as the coelomic pressure is varied
from one region of the body to another. The septa, as would be expected, bulge into
segments where the pressure is low but remain taut during all phases of contraction
and relaxation of the body-wall muscles. Any tension in the septal muscles will
obviously tend to prevent the transmission of changes of pressure from one segment
to the next, an effect favouring the localization of pressure changes and allowing of
differential pressures to be maintained in different parts of the body. This topic is
referred to again in the next section (p. 118).
With regard to the sphincter of the ventral foramen, it seems clear that in active
worms it is usually in a state of contraction and effectively closes the ventral foramen
so that the segmentally arranged coelomic compartments are isolated one from the
other in the sense that coelomic fluid cannot pass freely along the body. This
isolation of the fluid in the successive compartments can be clearly demonstrated by
the simple experiment of attempting to force fluid into the body of an active worm
by means of a hypodermic syringe. It is found that it is virtually impossible to inject
any quantity of fluid into the body until a force is applied sufficient to rupture the
septa. Yet, in a fully narcotized worm, fluid can be freely injected and causes the
whole body to become inflated even under a pressure as low as 15 cm. water.
In an attempt to confirm some of these observations a few coelomic compartments
in selected regions of the body were injected with a suspension of bismuth oxycarbonate. The worms so treated were then photographed by means of X-rays,
allowed to wriggle for a few minutes and again photographed. Although not good,
the photographs were sufficiently clear to show that the suspension remained confined to those segments into which it was originally injected, thus indicating that
during locomotion fluid does not pass between the coelomic compartments.
MEASUREMENTS OF PRESSURE IN THE COELOMIC FLUID
Compared with the lugworm the earthworm is a very active creature and the insertion of a hypodermic needle through the body wall evoked violent wriggling movements and usually completely upset the normal locomotory pattern. Nevertheless,
it was found possible to make a series of readings of the internal pressures by means
of a manometer filled with Hddon-Fleig's fluid and connected to the coelomic cavity
by means of a hypodermic needle in the same way as was used to measure pressures
in the lugworm (Chapman & Newell, 1947)- The pressures recorded in this way
were, within the limits of experimental error, the same as if the manometer were
filled with water and at least indicate the order of pressures inside the worms. The
results are given in Tables 1 and 2 whilst Table 3 is a record of pressures in worms
fully narcotized with 8% magnesium sulphate.
The hydrostatic pressures in the coelomic fluid in various regions of the body of
a fresh series of active worms was next measured by means of the glass spoon gauge
apparatus set up and calibrated in essentially the same way as that described by
The role of the coelomicfluidin the movements of earthworms
115
Table 1. Pressures in cm. of water recorded by means of a capillary manometer
at \ min. intervals in segment 28 of active worms
(Corrected for height of animal and capillary rise in the tube.)
Worm
no.
0
I
2
1
23-S
240
230
13-0
I9'O
13-5
2
3
4
5
6
7
8
9
10
11
12
2 2 0
22-0
22-O
22-O
22-O
4
5
ISO
15-0
19-0
180
17-0
16-0
I9-S
195
I7-O
I9-O
20 -o
2O-S
200
2O-O
23 0
23-O
19-0
2O-O
I9-O
2OO
20-0
14-0
2O-O
160
I4-0
23"5
I3-5
13-5
ISO
17-0
22-5
380
2S'O
2S-0
2S-O
3
23-S
22-O
22'0
19-0
2O-O
19-0
2O-0
21-5
2I-O
20-0
20-0
6
7
8
worm slipped off ne idle
14-0
150
13s
17-0
180
18-0
170
i6-o
17-0
i6-s
16-5
16-0
17-0
i3-5
150
i6-s
16-0
17-5
21 -o
130
17-0
2O-0
20-0
I7O
is-s
170
170
150
170
9
10
12-5
13-0
170
170
170
170
16-0
16-0
17-0
22'O
i65
i6S
i6-s
16-0
16-0
18-0
18-5
i8- S
16-0
17-0
2I-O
14-0
i6-s
i3'S
iS'S
i5'S
i3'5
14-5
i9S
13-5
io-o
15-5
16-0
160
140
16-0
150
16s
Mean of initial pressures, 24-5 cm. water. Mean pressure in twelve worms, 17-5 cm. water.
Mean of pressures after 5 min., 16-0 cm. water.
Table 2. Pressures in cm. of water recorded by means of a capillary manometer
at £ min. intervals in tail region of active worms
Worm
no.
0
1
2
180
2O'O
I9-O
19-0
19-0
180
II-O
8-o
16-0
14-0
15-0
12-0
12-0
90
1
250
2
25-0
3
4
S
250
250
250
250
6
3
4
IO'O
95
II-O
IO-O
60
80
5
6
7
8
9
10
5-5
5'O
60
SO
SO
4'S
S-o
4-S
4-S
6-o
5-o
40
SO
40
S-5
SO
S'O
4-5
4-5
S-o
SO
4-0
4-S
7-0
7-0
80
60
7'5
8-5
6-5
7'5
6-o
S-o
6-S
S-o
4-5
S-o
4-S
4-5
S-o
Mean pressure in six worms 8-o cm. water.
Table 3. Pressure in cm. of water recorded by means of a capillary manometer
at \ min. intervals in segnient 28 of anaesthetized worms
Worm
no.
1
0
S-o
2
1 0 0
3
io-o
I
2
40
i-o
3-0
o-S
2-S
2-0
I-O
4
IO'O
2-O
S
io-o
30
6
80
2-0
i-S
i-o
4
3
S
6
7
8
9
10
3'O
30
3-0
3-0
3-o
30
30
30
0
0
0
0
0
0
0
0
i-o
i-o
i-o
i-o
0
0
0
0
0
0
o-S
0
0
0
0
0
0
0-5
0
0
0
0
0
0
o-S
0
0
0
0
0
0
0
Except for worm no. 1, which revived slightly at the beginning of the experiment, pressures fell
to zero at the end of 2$ min.
Picken (1936). A few trial readings sufficed to show that, as suspected, the measurements of coelomic pressures in the earthworm by means of a manometer is open to
certain objections for, owing to the small amount of fluid in each coelomic compartment, an apparatus which will register differences in pressure under virtually
8-a
n6
G. E. NEWELL
isometric conditions is desirable. Also, it was apparent that the internal pressure
changes vary rapidly so that a practically instantaneous recording is required.
Spoon gauges satisfy both these conditions.
As in previous recordings, the apparatus was placed in communication with the
body cavity of the worm by a hypodermic needle inserted through the body wall.
The results of two series of readings are given in Tables 4 and 5.
Table 4. Pressures in cm. of water recorded at J and \ min. intervals
by means of a spoon gauge in the anterior third of active worms
Series 1. Pressures recorded at i min. intervals.
Worm
no.
1
0
2
3
25-0 23-0 i6'o
25-0 24-0 18-0
as-o 25-0 14-0
2S'O 2 S O 2 2 0
2S-0 22-0 1 0 0
2 5 0 24'O 1 6 0
1
2
3
4
0
4
I(J'O
24-0
2S'O 14-0
1 4 0 IO'O
18-0 I2'O
IO'O
8'O
80
220
6
5
8
7
8-0 16-o i6'o
100
2S'O
8-o 1 0 0 14-0
IO'O
17-0
18-0
i6'0 14-0 14-0
13-0 1 8 0
140
ao'o
150
IO'O
n
10
9
24O
IO'O
I2'0
I7'0
JO'O
II'O
8-o
140
17-0
II'O
12
13
16
•5
14
18
17
Worm slipped off needle
Worm slipped off needle
•SO 18-o IO'O
Slipped off needle
200
160
29'O
IO'O
8-o
n o 14-0 i8'0
18-o
18-0
S'O
II'O
80
100
8-o
II'O
16-0 IA'O ib'O
i6'O IO'O 8-o 1 2 0
ia-o IO'O i6'O IO'O
22'0
IO'O
i6'0
80
Mean pressure in six worms, 15*0 cm, water.
Series a. Pressures recorded at t min. intervals.
Worm
no.
i
2
3
4
0
1
27'0
27'O
27'0
1
I9
3S-0
3S-o
3S-0
3S-0
IO
3S"O
3
4
150
IO'O
IO'O
120
120
I2'O
13-0
a-o
2'O
2 0
I2'O
30
150
5'°
i6'o
70
220
i6'O
140
80
30
IO'O
no
120
130
25-0
20
9'O
25'O
30
14-0
I2'O
J2'O
30
9-0
2JO
2'O
I2'O
220
22O
iS'O
5
7-o
300
7
8
9
70
S'O
170
170
2-O
10
Worm slipped ol ' needle
IO'O
18-0
70
20
IO'O
90
I2'O
35-o
6
2
Mean pressure in nine worms, ia*o cm. water.
series 1 and a, 1 3 5 cm. water.
3-0
17-0
i6'O
5'°
130
4-0
So
140
14-0
30-0
160
240
12-0
120
180
120
220
160
r°
170
IO'O
i6'O
so
50
S'O
aj-o
15-0
2S'O
50
120
S'O
3'0
100
SO
I2-O
2O'O
200
Worms nos. 3 and 7 appeared very sluggish. Average pressure from
Table 5. Pressures in cm. of water recorded at J and \ min. intervals
by means of a spoon gauge in the tail region of active worms
Series i. Pressures recorded at J min. intervals.
Worm
no.
1
2
3
0
I
2
3
4
S
6
7
8
9
10
11
12
250
250
25-0
14-0
14-0
16-0
140
80
14-0
80
IO'O
140
160
70
80
II'O
190
90
60
8-o
50
60
80
I4'O
8.0
60
IO'O
120
60
IO'O
II'O
7-o
7-o
IO'O
IO'O
70
i6'0
80
60
Mean pressure in three worms, io-o cm. water.
Series 2. Pressures recorded at i min. intervals.
Worm
no.
1
2
3
0
1
2S'O
25-0
25-0
IO'O
II'O
i6-o
2
8'O
70
80
3
4
5
6
7
8
9
10
II
12
70
60
90
7-0
70
80
90
80
80
60
70
60
70
70
40
70
80
40
70
40
SO
60
40
40
60
70
6O
Mean pressure in three worms, 7-0 cm. water.
7'O
Average from series 1 and 2, 8-5 cm. water.
The role of the coelomicfluidin the movements of earthworms
117
DISCUSSION OF RESULTS
From Tables 4 and 5 it will be seen that in the anterior third of the body of an
actively wriggling earthworm there is an average hydrostatic pressure of about
13-5 cm. water, but that this pressure is subject to considerable and fairly rapid
changes, falling as low as 2-0 cm. water and rising as high as 29 cm. water. The
figures for the tail end of active worms are lower, the mean pressure being 8-5 cm.
water and the fluctuation being from 4 to 19 cm. water. The pressures measured in
the second series of worms were lower than in the first series, and this result is
probably due to the worms being less active.
The mean pressures recorded both for the anterior and tail regions of the body
are in good agreement with those measured by means of the capillary manometer,
but show more clearly how the pressure fluctuates. The manometer readings
showed a gradual fall over a period of time with practically no fluctuations, and
whilst it is true that, on the whole, the readings taken with the spoon gauge were also
lower towards the ends of the series and that the readings did not extend over such
a long period of time, the significant feature is the recording of large fluctuations of
pressure.
It was found difficult to correlate in any precise way the changes in pressure with
definite muscular configurations, but it was noted that the highest pressures
occurred when the circular muscles were fully contracted. A state of moderate
relaxation of both sets of body-wall muscles is associated with low hydrostatic
pressures whilst, as is shown in Table 3, the pressure in narcotized worms is zero.
The general fall in pressure towards the ends of the series of recordings may,
perhaps, be accounted for by the fatigue of the body-wall muscles, whilst the lower
mean obtained from the measurements with the spoon gauge when compared with
manometric measurements seems to be due to the fluctuations. It seems certain
that the pressure in worms connected to a manometer is steadied by fluid entering
the body cavity from the manometer, and also because the amount of fluid in any
one coelomic compartment is small when compared with the volume in the apparatus.
Variations in pressure are therefore smoothed out in a way not possible with a practically isometric apparatus like the spoon gauge.
THE FORCES DEVELOPED DURING LOCOMOTION
It seems fair to assume that, as in the lugworm, the forces available to an earthworm
for developing a forward thrust and for causing changes in the shape of the body are
brought about by the interaction of the body-wall muscles and coelomic fluid, and
that an estimate of these forces can be arrived at indirectly by calculation from the
pressures recorded. The pressure in the coelomic fluid will be distributed uniformly,
and when the circular muscles of the body wall contract the body will become
extended with a force proportional to the pressure and to the cross-sectional area in
the region of the body under consideration. Conversely, when the longitudinal
muscles contract and the circulars relax, the diameter of the body will be increased
by the pressure making itself apparent by forces acting radially. It is clear that
n8
G. E. NEWELL
since the septa do not behave as rigid partitions the pressure in any one segment
cannot exceed that in a neighbouring segment without causing the septum to bulge.
Any tension in the septal muscles will, however, cause resistance to bulging, and the
cumulative effect of the resistance of several septa is appreciable and allows of
pressure differences to be set up and maintained in different parts of the body. This
effect was tested by connecting a spoon gauge to the coelom in the anterior third of
the body so that pressure could be measured whilst, at the same time, saline solution
was forced into the coelom in the clitellar region by means of a hypodermic syringe.
It was found that the pressure in the anterior third rose only very slightly (by about
i cm. water, in fact) until the pressure set up by the syringe was sufficient to rupture
the septa and to drive fluid forwards into the segments in which pressures were
being measured.
It has already been demonstrated that the septa divide the body of an earthworm
into functional fluid-tight compartments so that alterations in the shape of the body
must be brought about solely by the contractions of the individual segments and are
not, as in some worms, accompanied by movements of fluid from one part of the
body to another. Further, any thrust exerted by the extreme anterior end of the
worm when the body is elongating, must be equal to the total force applied by the
coelomic fluid to the first septum (i.e. that separating segment 4 from segment 5),
the first four segments, in which the body cavity is virtually occluded, acting as
a solid muscular organ. In the worms examined, the highest pressure recorded in
the anterior third of the body was 29 cm. water and, neglecting the two sluggish
specimens, the lowest was 5 cm. water. An average figure for the diameter of the
body in the region of the first septum is about 07 cm. when the circular muscles are
fully relaxed. In this region of the body the gut has a diameter of about 0-35 cm. so
that the area of the first septum is
3-14xo-352 —3-14x0-17* = 0-295 sq.cm.
The force acting on the septum causing it to bulge forwards and transmit pressure
to the segments in front was, in this instance, equal to 29 x 0-295 = 8"5 g- It is of
interest to note that this figure, arrived at very indirectly, agrees well with the upper
figure given by Gray & Lissmann (19386), who measured the forces by means of
a special torsion balance. Gray & Lissmann gave the range of forces as from 2 to 8 g.,
and from the lowest figure for pressures in the anterior third of the body, namely,
5 cm. water, a thrust of 1.5 g. can be calculated which again is a good agreement with
the figures obtained by direct measurement.
Forces of this order probably suffice to allow earthworms to burrow into and
through soils of varying resistance, even quite heavy clays, but of importance in
forcing a way through the soil is the actual pressure which can be applied by the
conical front end of the body. If, for example, the diameter of the prostomium
which forms the apex of a cone, the rest of which is formed by the first four
segments, is i-o mm., then its area is 0-008 sq.cm. Assuming as before that the force
applied to the first septum is equivalent to 8-5 g., then the pressure of the prostomium against the soil will be 8-5/0-008 = 1060 g./sq.cm.
The role of the coelomicfluidin the movements of earthworms
119
When burrowing, the pointed anterior end of the body is forced into any crevices
between the soil particles, and the gap is then widened by inflation of that part of the
body which has entered below the surface. Pressures have not been recorded during
this phase of activity but are probably much higher than any obtained during
wriggling, since they would be due to the contraction of the powerful longitudinal
muscles of the body wall which, as can be seen in cross-section, are far more bulky
than the circular muscles. When the worm is on the surface the longitudinal
musculature cannot, of course, generate a pressure in the coelomic fluid greater than
can be withstood by the circular muscles of the body wall. On the other hand, when
a worm is in its burrow the body wall will be prevented from undue expansion or
bursting by the walls of the burrow, and this may allow the longitudinal muscles to
raise the pressure in the coelom to much higher levels than have been recorded in
this investigation. Penetration of the anterior end of the body into the soil is often
accompanied by a to-and-fro rotation of the anterior end of the body in much the
same way as a bradawl is used for boring into wood. This movement aids in the
loosening of soil particles. Then, once a portion of the body has entered the soil the
worm can get a grip on the sides of the burrow and the rest of the body can be drawn
inwards and the burrow be gradually extended.
It will be seen that a watertight septate construction of the body is favourable to
the mechanism of crawling as described by Gray & Lissmann (1938a) in which an
essential feature is the contraction of the longitudinal muscles of a few segments to
form a 'foot' or point d'appui which resists the reaction to a forward thrust by the
anterior end of the body and also the reaction to the tension which drags forward the
posterior end of the body of the worm.
Chapman (1949)* points out that in a cylindrical, fluid-filled animal the constriction of the circular muscles at one end would produce an effect on the shape of the
body dependent on the tensions in the circular and longitudinal muscles in other
regions, and only if the pressures exerted by these latter muscles on the coelomic
fluid exceeds that exerted by the longitudinal muscles of the constricting region,
would that end necessarily elongate.
On the other hand, if the body is divided into separate regions by septa which can
actively resist the pressures produced by contraction of the body-wall muscles, then
contraction of the circular muscles may produce effects which can be confined to
particular regions of the body. For example, in a crawling earthworm the contraction
of the longitudinal muscles in the region of the point d'appui would have the effect
of stretching the septa since they are watertight and the diameter of the body will
increase. In the region anterior to the point d'appui, which is elongating because of
the contraction of the circular muscles, the pressure can be high (since only by an
increased pressure can the contraction of the circular muscles be translated into
movement). On the other hand, the pressure in the region posterior to the point
d'appui need only be low, since the tail is being passively dragged forward by the
contraction of the longitudinal muscles for whose action no intervention of a fluid
transmission system is necessary. Were it not for the septate construction of the body
• Private communication.
120
G.
E.
NEWELL
it is difficult to see how it would be possible simultaneously to extend the anterior
end by increased pressure and to retract the posterior end at reduced pressure.
THE MECHANISM FOR THE PREVENTION OF LEAKAGE
OF COELOMIC FLUID
To any animal whose locomotion and turgidity depends on a body-wall muscle-body
fluid system and which may be said therefore to possess a hydrostatic skeletal
system, it is clearly essential that there shall be no uncontrolled escape of fluid
through any pores or ducts which lead from the coelom to the exterior. This is
particularly true of a terrestrial animal such as the earthworm which is frequently
faced with the danger of desiccation by mere evaporation from the surface of the
body. It is not surprising to find, therefore, that the nephridiopores and dorsal pores
are provided with sphincters which effectively control the outward passage of
coelomic fluid under the range of pressures normally found in active worms.
Even in the lugworm the nephridiopores open only rather rarely to allow of voiding
of the urine—every 5 sec. according to Strunk (1930)—whilst an old observation of
Cu6not (1898) gives the rate of opening of the nephriodipores of the earthworm as
once every 3 days. This has not, apparently, been confirmed, but a smaller quantity
of urine is to be expected in a land animal where conservation of water is often of
importance.
In order to test at what pressure leakage of the coelomic fluid occurs, a worm was
bisected and a canula was then inserted at the cut end to one side of the gut.
A ligature around the body and canula sufficed to make a pressure-tight joint. The
canula was then connected to a manometer filled with H^don-Fleig's fluid by which
means the pressure was increased by 10 cm. of water at a time and allowed to remain
at each pressure for i | min. to allow the apertures to be observed for leakage. No
leakage was observed even when the pressure was raised to 150 cm. of water which is
well above the normal working range.
A pressure of a mere 20 cm. of water is, however, sufficient to cause water to
spurt from the dorsal pores of a narcotized worm. Even in narcotized specimens,
however, the nephridiopores and gonoducts did not leak under high pressures, since
their internal apertures seemed to act as valves which close when the internal
pressure rises.
SUMMARY
1. A short review is given of the coelom and of its morphological relations in the
earthworm.
2. The arrangement of the intrinsic muscles in a typical septum is described.
Four main sets of muscles are recognized: viz. radial muscles, circular muscles,
oblique muscles, and the sphincter around the ventral foramen.
3. It is suggested that the function of the radial, circular and possibly of the
oblique muscles is to control bulging of the septa, and so serve to localize differences
in pressure in the coelomic fluid. Normally, in active worms, the sphincter of the
ventral foramen is contracted and forms an effective barrier to the passage of fluid
The role of the coelomic fluid in the movements of earthworms
121
from one coelomic compartment to the next. This was verified experimentally and
by X-ray photography.
4. A series of measurements of the pressure in the coelomic fluid in different
regions of active worms was recorded by means of a capillary manometer and by the
use of a spoon-gauge apparatus. Manometric measurements showed the average
pressure in the anterior third of the body to be 16-0 cm. water and in the tail region
to be 8-o cm. water. The corresponding figures obtained with a spoon gauge were
13-5 and 8-5 cm. water. The pressure in narcotized worms is zero.
5. These results are discussed, and it is pointed out that the manometer readings
suffer from the disadvantage of failing to show the rapid fluctuations in pressure
which occur during wriggling movements of the worms.
6. It is calculated from these pressure readings that a worm can exert a forward
thrust equivalent to forces of between 1-5 and 8-o g. These figures agree well with
those obtained by Gray & Lissman by the use of a special torsion balance.
7. The burrowing movements of earthworms are briefly described.
8. It is shown that the sphincters of the dorsal pores and of the nephridiopores do
not normally allow of the escape of coelomic fluid, and will withstand a pressure well
outside the normal range.
REFERENCES
BOHN, G. (1901). Bull. Mus. Hilt, nat., Paris, 7, 404.
CUENOT, L. (1898). Arch. Biol., Paris, 15, 79.
CHAPMAN, G. & NEWELL, G. E. (1947). Proc. Roy. Soc. B, 134, 431.
DARWIN, C. (1881). The formation of vegetable mould through the action of worms with some observations
on their habits. London.
FHIEDLANDER, B. (1894). Cited by STEVENSON, J. (1930). The Oligochaeta. Oxford.
GRAY, J. & LISSMANN, H. W. (1938a). J. Exp. Biol. 15, 506.
GRAY, J. & LISSMANN, H. W. (19386). J. Exp. Biol. 15, 318.
PICKEN, L. E. R. (1936). J. Exp. Biol. 13, 309.
RIBAUCOURT, E. DE (1901). Bull. set. Fr. Belg. 35, 211.
STRONK, C. (193°)- Zool. J. (Abt. 3), 47, 259-